Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2446-2456

  Chattha, Kuldeep S ^a   Vlasova, Anastasia N ^a   Kandasamy, Sukumar ^a   Rajashekara, Gireesh ^a   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 8; PROBIOTIC AGENT; ROTAVIRUS VACCINE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BIFIDOBACTERIUM ANIMALIS; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; DIARRHEA; DRUG POTENTIATION; IMMUNOMODULATION; IMMUNOREGULATION; LACTOBACILLUS RHAMNOSUS; NEWBORN; NONHUMAN; PIGLET; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; ROTAVIRUS INFECTION; T LYMPHOCYTE; VIRUS SHEDDING;

ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GERM-FREE LIFE; HUMANS; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; PROBIOTICS; ROTAVIRUS INFECTIONS; ROTAVIRUS VACCINES; SWINE; T-LYMPHOCYTES;

EID: 84883405129     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300678     Document Type: Article

References (68)

1. Tate, J. E., A. H. Burton, C. Boschi-Pinto, A. D. Steele, J. Duque, U. D. Parashar; WHO-coordinated Global Rotavirus Surveillance Network. 2012. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 12: 136-141.
2. Gray, J. 2011. Rotavirus vaccines: safety, efficacy and public health impact. J. Intern. Med. 270: 206-214.
3. Licciardi, P. V., and M. L. Tang. 2011. Vaccine adjuvant properties of probiotic bacteria. Discov. Med. 12: 525-533.
4. Preidis, G. A., C. Hill, R. L. Guerrant, B. S. Ramakrishna, G. W. Tannock, and J. Versalovic. 2011. Probiotics, enteric and diarrheal diseases, and global health. Gastroenterology 140: 8-14.
5. Fanaro, S., R. Chierici, P. Guerrini, and V. Vigi. 2003. Intestinal microflora in early infancy: composition and development. Acta Paediatr. Suppl. 91: 48-55.
6. Rinne, M., M. Kalliomaki, H. Arvilommi, S. Salminen, and E. Isolauri. 2005. Effect of probiotics and breastfeeding on the bifidobacterium and lactobacillus/enterococcus microbiota and humoral immune responses. J. Pediatr. 147: 186-191.
7. Sjogren, Y. M., S. Tomicic, A. Lundberg, M. F. Bottcher, B. Bjorksten, E. Sverremark-Ekstrom, and M. C. Jenmalm. 2009. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin. Exp. Allergy 39: 1842-1851.
8. Saavedra, J. M., N. A. Bauman, I. Oung, J. A. Perman, and R. H. Yolken. 1994. Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. Lancet 344: 1046-1049.
9. Szajewska, H., M. Kotowska, J. Z. Mrukowicz, M. Armánska, and W. Mikołajczyk. 2001. Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants. J. Pediatr. 138: 361-365.
10. Delcenserie, V., D. Martel, M. Lamoureux, J. Amiot, Y. Boutin, and D. Roy. 2008. Immunomodulatory effects of probiotics in the intestinal tract. Curr. Issues Mol. Biol. 10: 37-54.
11. Hooper, L. V., D. R. Littman, and A. J. Macpherson. 2012. Interactions between the microbiota and the immune system. Science 336: 1268-1273.
12. Atarashi, K., T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, Y. Momose, G. Cheng, S. Yamasaki, T. Saito, Y. Ohba, et al. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341.
13. Ivanov, I. I., K. Atarashi, N. Manel, E. L. Brodie, T. Shima, U. Karaoz, D. Wei, K. C. Goldfarb, C. A. Santee, S. V. Lynch, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498.
14. Cho, I., S. Yamanishi, L. Cox, B. A. Methé, J. Zavadil, K. Li, Z. Gao, D. Mahana, K. Raju, I. Teitler, et al. 2012. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488: 621-626.
15. Ward, L. A., B. I. Rosen, L. Yuan, and L. J. Saif. 1996. Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs. J. Gen. Virol. 77: 1431-1441.
16. Azim, T., S. M. Ahmad, Sefat-E-Khuda, M. S. Sarker, L. E. Unicomb, S. De, J. D. Hamadani, M. A. Salam, M. A. Wahed, and M. J. Albert. 1999. Immune response of children who develop persistent diarrhea following rotavirus infection. Clin. Diagn. Lab. Immunol. 6: 690-695.
17. Jiang, B., L. Snipes-Magaldi, P. Dennehy, H. Keyserling, R. C. Holman, J. Bresee, J. Gentsch, and R. I. Glass. 2003. Cytokines as mediators for or effectors against rotavirus disease in children. Clin. Diagn. Lab. Immunol. 10: 995-1001.
18. Azevedo, M. S., L. Yuan, S. Pouly, A. M. Gonzales, K. I. Jeong, T. V. Nguyen, and L. J. Saif. 2006. Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. J. Virol. 80: 372-382.
19. Xu, J., Y. Yang, J. E. Sun, Y. Z. Ding, L. Y. Su, and C. H. Shao. 2007. Expression of Toll-like receptors in mononuclear cells from children with acute rotavirus diarrhea. Chinese Journal of experimental and clinical virology. 21: 38-40.
20. Wen, K., M. S. Azevedo, A. Gonzalez, W. Zhang, L. J. Saif, G. Li, A. Yousef, and L. Yuan. 2009. Toll-like receptor and innate cytokine responses induced by lactobacilli colonization and human rotavirus infection in gnotobiotic pigs. Vet. Immunol. Immunopathol. 127: 304-315.
21. Wen, K., G. Li, T. Bui, F. Liu, Y. Li, J. Kocher, L. Lin, X. Yang, and L. Yuan. 2012. High dose and low dose Lactobacillus acidophilus exerted differential immune modulating effects on T cell immune responses induced by an oral human rotavirus vaccine in gnotobiotic pigs. Vaccine 30: 1198-1207.
22. Zhang, W., M. S. Azevedo, K. Wen, A. Gonzalez, L. J. Saif, G. Li, A. E. Yousef, and L. Yuan. 2008. Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 26: 3655-3661.
23. Zhang, W., M. S. Azevedo, A. M. Gonzalez, L. J. Saif, T. Van Nguyen, K. Wen, A. E. Yousef, and L. Yuan. 2008. Influence of probiotic Lactobacilli colonization on neonatal B cell responses in a gnotobiotic pig model of human rotavirus infection and disease. Vet. Immunol. Immunopathol. 122: 175-181.
24. Maidens, C., C. Childs, A. Przemska, I. B. Dayel, and P. Yaqoob. 2013. Modulation of vaccine response by concomitant probiotic administration. Br. J. Clin. Pharmacol. 75: 663-670.
25. Chattha, K. S., A. N. Vlasova, S. Kandasamy, M. A. Esseili, C. Siegismund, G. Rajashekara, and L. J. Saif. 2013. Probiotics and colostrum/milk differentially affect neonatal humoral immune responses to oral rotavirus vaccine. Vaccine 31: 1916-1923.
26. Meyer, R. C., E. H. Bohl, and E. M. Kohler. 1964. Procurement and maintenance of germ-free seine for microbiological investigations. Appl. Microbiol. 12: 295-300.
27. Yuan, L., L. A. Ward, B. I. Rosen, T. L. To, and L. J. Saif. 1996. Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J. Virol. 70: 3075-3083.
28. Yuan, L., K. Wen, M. S. Azevedo, A. M. Gonzalez, W. Zhang, and L. J. Saif. 2008. Virus-specific intestinal IFN-gamma producing T cell responses induced by human rotavirus infection and vaccines are correlated with protection against rotavirus diarrhea in gnotobiotic pigs. Vaccine 26: 3322-3331.
29. Pérez-Cano, F. J., S. Marín-Gallén, M. Castell, M. Rodríguez-Palmero, M. Rivero, C. Castellote, and A. Franch. 2008. Supplementing suckling rats with whey protein concentrate modulates the immune response and ameliorates rat rotavirus-induced diarrhea. J. Nutr. 138: 2392-2398.
30. Guandalini, S., L. Pensabene, M. A. Zikri, J. A. Dias, L. G. Casali, H. Hoekstra, S. Kolacek, K. Massar, D. Micetic-Turk, A. Papadopoulou, et al. 2000. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J. Pediatr. Gastroenterol. Nutr. 30: 54-60.
31. Guarino, A., R. B. Canani, M. I. Spagnuolo, F. Albano, and L. Di Benedetto. 1997. Oral bacterial therapy reduces the duration of symptoms and of viral excretion in children with mild diarrhea. J. Pediatr. Gastroenterol. Nutr. 25: 516-519.
32. Isolauri, E., M. Juntunen, T. Rautanen, P. Sillanaukee, and T. Koivula. 1991. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
33. Rosenfeldt, V., K. F. Michaelsen, M. Jakobsen, C. N. Larsen, P. L. Møller, M. Tvede, H. Weyrehter, N. H. Valerius, and A. Paerregaard. 2002. Effect of probiotic Lactobacillus strains on acute diarrhea in a cohort of nonhospitalized children attending day-care centers. Pediatr. Infect. Dis. J. 21: 417-419.
34. Sherman, P. M., J. C. Ossa, and K. Johnson-Henry. 2009. Unraveling mechanisms of action of probiotics. Nutr. Clin. Pract. 24: 10-14.
35. Rodrigues, D. M., A. J. Sousa, K. C. Johnson-Henry, P. M. Sherman, and M. G. Gareau. 2012. Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. J. Infect. Dis. 206: 99-109.
36. Roselli, M., A. Finamore, S. Nuccitelli, P. Carnevali, P. Brigidi, B. Vitali, F. Nobili, R. Rami, I. Garaguso, and E. Mengheri. 2009. Prevention of TNBSinduced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of gammadeltaT and regulatory T cells of intestinal intraepithelial lymphocytes. Inflamm. Bowel Dis. 15: 1526-1536.
37. Kajander, K., K. Hatakka, T. Poussa, M. Färkkilä, and R. Korpela. 2005. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment. Pharmacol. Ther. 22: 387-394.
38. Kekkonen, R. A., N. Lummela, H. Karjalainen, S. Latvala, S. Tynkkynen, S. Jarvenpaa, H. Kautiainen, I. Julkunen, H. Vapaatalo, and R. Korpela. 2008. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J. Gastroenterol. 14: 2029-2036.
39. O'Mahony, C., P. Scully, D. O'Mahony, S. Murphy, F. O'Brien, A. Lyons, G. Sherlock, J. MacSharry, B. Kiely, F. Shanahan, and L. O'Mahony. 2008. Commensal-induced regulatory T cells mediate protection against pathogenstimulated NF-kappaB activation. PLoS Pathog. 4: e1000112.
40. Zhong, Y., A. Cantwell, and P. H. Dube. 2010. Transforming growth factor beta and CD25 are important for controlling systemic dissemination following Yersinia enterocolitica infection of the gut. Infect. Immun. 78: 3716-3725.
41. McNeal, M. M., S. C. Stone, M. Basu, J. D. Clements, A. H. Choi, and R. L. Ward. 2007. IFN-gamma is the only anti-rotavirus cytokine found after in vitro stimulation of memory CD4+ T cells from mice immunized with a chimeric VP6 protein. Viral Immunol. 20: 571-584.
42. Jaimes, M. C., O. L. Rojas, A. M. González, I. Cajiao, A. Charpilienne, P. Pothier, E. Kohli, H. B. Greenberg, M. A. Franco, and J. Angel. 2002. Frequencies of virusspecific CD4(+) and CD8(+) T lymphocytes secreting gamma interferon after acute natural rotavirus infection in children and adults. J. Virol. 76: 4741-4749.
43. Mesa, M. C., L. Gutiérrez, C. Duarte-Rey, J. Angel, and M. A. Franco. 2010. A TGF-beta mediated regulatory mechanism modulates the T cell immune response to rotavirus in adults but not in children. Virology 399: 77-86.
44. Dong, H., I. Rowland, and P. Yaqoob. 2012. Comparative effects of six probiotic strains on immune function in vitro. Br. J. Nutr. 108: 459-470.
45. Kaji, R., J. Kiyoshima-Shibata, M. Nagaoka, M. Nanno, and K. Shida. 2010. Bacterial teichoic acids reverse predominant IL-12 production induced by certain lactobacillus strains into predominant IL-10 production via TLR2-dependent ERK activation in macrophages. J. Immunol. 184: 3505-3513.
46. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9: 4-9.
47. Zaghouani, H., C. M. Hoeman, and B. Adkins. 2009. Neonatal immunity: faulty T-helpers and the shortcomings of dendritic cells. Trends Immunol. 30: 585-591.
48. Chen, C. Y., D. Huang, S. Yao, L. Halliday, G. Zeng, R. C. Wang, and Z. W. Chen. 2012. IL-2 simultaneously expands Foxp3+ T regulatory and T effector cells and confers resistance to severe tuberculosis (TB): implicative Treg-T effector cooperation in immunity to TB. J. Immunol. 188: 4278-4288.
49. Wen, K., G. Li, X. Yang, T. Bui, M. Bai, F. Liu, J. Kocher, and L. Yuan. 2012. CD4+ CD25- FoxP3+ regulatory cells are the predominant responding regulatory T cells after human rotavirus infection or vaccination in gnotobiotic pigs. Immunology 137: 160-171.
50. Meijerink, M., and J. M. Wells. 2010. Probiotic modulation of dendritic cells and T cell responses in the intestine. Benef. Microbes 1: 317-326.
51. Flinterman, A. E., E. F. Knol, A. G. van Ieperen-van Dijk, H. M. Timmerman, A. C. Knulst, C. A. Bruijnzeel-Koomen, S. G. Pasmans, and E. van Hoffen. 2007. Probiotics have a different immunomodulatory potential in vitro versus ex vivo upon oral administration in children with food allergy. Int. Arch. Allergy Immunol. 143: 237-244.
52. O'Flaherty, S., D. M. Saulnier, B. Pot, and J. Versalovic. 2010. How can probiotics and prebiotics impact mucosal immunity? Gut Microbes 1: 293-300.
53. Imaoka, A., T. Shima, K. Kato, S. Mizuno, T. Uehara, S. Matsumoto, H. Setoyama, T. Hara, and Y. Umesaki. 2008. Anti-inflammatory activity of probiotic Bifidobacterium: enhancement of IL-10 production in peripheral blood mononuclear cells from ulcerative colitis patients and inhibition of IL-8 secretion in HT-29 cells. World J. Gastroenterol. 14: 2511-2516.
54. López, P., I. González-Rodríguez, M. Gueimonde, A. Margolles, and A. Suárez. 2011. Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity. PLoS ONE 6: e24776.
55. Pohjavuori, E., M. Viljanen, R. Korpela, M. Kuitunen, M. Tiittanen, O. Vaarala, and E. Savilahti. 2004. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow's milk allergy. J. Allergy Clin. Immunol. 114: 131-136.
56. Ruiz, P. A., M. Hoffmann, S. Szcesny, M. Blaut, and D. Haller. 2005. Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats. Immunology 115: 441-450.
57. Lu, W., S. Chen, C. Lai, W. Guo, L. Fu, and J. M. Andrieu. 2012. Induction of CD8(+) regulatory T cells protects macaques against SIV challenge. Cell Rep. 2: 1736-1746.
58. Silva-Campa, E., V. Mata-Haro, E. Mateu, and J. Hernández. 2012. Porcine reproductive and respiratory syndrome virus induces CD4+CD8+CD25+Foxp3+ regulatory T cells (Tregs). Virology 430: 73-80.
59. Jiang, H., S. M. Canfield, M. P. Gallagher, H. H. Jiang, Y. Jiang, Z. Zheng, and L. Chess. 2010. HLA-E-restricted regulatory CD8(+) T cells are involved in development and control of human autoimmune type 1 diabetes. J. Clin. Invest. 120: 3641-3650.
60. McNeal, M. M., M. Basu, J. A. Bean, J. D. Clements, N. Y. Lycke, A. Ramne, B. Löwenadler, A. H. Choi, and R. L. Ward. 2007. Intrarectal immunization of mice with VP6 and either LT(R192G) or CTA1-DD as adjuvant protects against fecal rotavirus shedding after EDIM challenge. Vaccine 25: 6224-6231.
61. Crowe, C. R., K. Chen, D. A. Pociask, J. F. Alcorn, C. Krivich, R. I. Enelow, T. M. Ross, J. L. Witztum, and J. K. Kolls. 2009. Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 183: 5301-5310.
62. Ryzhakov, G., C. C. Lai, K. Blazek, K. W. To, T. Hussell, and I. Udalova. 2011. IL-17 boosts proinflammatory outcome of antiviral response in human cells. J. Immunol. 187: 5357-5362.
63. Gaffen, S. L. 2009. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 9: 556-567.
64. Round, J. L., and S. K. Mazmanian. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9: 313-323.
65. Smith, K., K. D. McCoy, and A. J. Macpherson. 2007. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19: 59-69.
66. Desselberger, U., and H. I. Huppertz. 2011. Immune responses to rotavirus infection and vaccination and associated correlates of protection. J. Infect. Dis. 203: 188-195.
67. Yuan, L., and L. J. Saif. 2002. Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet. Immunol. Immunopathol. 87: 147-160.
68. Silva, A. M., E. A. Bambirra, A. L. Oliveira, P. P. Souza, D. A. Gomes, E. C. Vieira, and J. R. Nicoli. 1999. Protective effect of bifidus milk on the experimental infection with Salmonella enteritidis subsp. typhimurium in conventional and gnotobiotic mice. J. Appl. Microbiol. 86: 331-336.